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Whipple was born on November 5, 1906, in Red Oak, Iowa, as the son of a farmer. An early bout with polio ended his ambition of being a professional tennis player. Whipple studied at Occidental College in Southern California, then majored in mathematics at the University of California at Los Angeles, graduating in 1927. Recollecting his path from mathematics to astronomy, Whipple stated in a 1978 autobiography that his "mathematics major veered [him] through physics and finally focused on astronomy where time, space, mathematics, and physics had a common meeting ground."[2]

From 1950 until 1977 he was a professor of Astronomy at Harvard University, including being the Phillips Professor of Astronomy between 1968 and 1977. During these years (in the early 1950s), he wrote a series of influential papers entitled A Comet Model, published in Astrophysical Journal.[3][4][5] In these papers, he proposed the "icy conglomerate" hypothesis of comet composition (later called the "dirty snowball" hypothesis). The basic features of this hypothesis were later confirmed; however, the exact amount (and thus the importance) of ices in a comet is an active field of research, with most of the recently obtained data[6] pointing to a low contribution of ices to a comet's mass (dubbed the "icy dirtball" hypothesis). He also anticipated the era of artificial satellites and organized the members of Operation Moonwatch to track them. These groups were the only ones in the US prepared and ready to make observations when the Soviet Union unexpectedly launched Sputnik I in 1957. He became director of the Smithsonian Astrophysical Observatory when Loyal Blaine Aldrich retired in 1955,[7] and remained in this post until 1973.

Whipple made at least one media appearance, in the science documentary film Target...Earth? (1980). He also appeared in the BBC's coverage of the Giotto encounter with Halley's Comet, in 1986.